This page intentionally left blank Lichen Biology Lichens are symbiotic organisms in which fungi and algae and/or cyanobacteria form an intimate biological union. This diverse group is found in almost all terrestrial habitats from the tropics to polar regions. In this second edition, four completely new chapters cover recent developments in the study of these fascinating organisms, including lichen genetics and sexual reproduction, stress physiology and symbiosis, and the carbon economy and environmental role of lichens. The whole text has been fully updated, with chapters covering anato- mical, morphological and developmental aspects; the chemistry of the unique secondary metabolites produced by lichens and the contribution of these sub- stances to medicine and the pharmaceutical industry; patterns of lichen photosynthesis and respiration in relation to different environmental condi- tions; the role of lichens in nitrogen fixation and mineral cycling; geographical patterns exhibited by these widespread symbionts; and the use of lichens as indicators of air pollution. This is a valuable reference for both students and researchers interested in lichenology. T H O M A S H . N A S H I I I is Professor of Plant Biology in the School of Life Sciences at Arizona State University. He has over 35 years teaching experience in Ecology, Lichenology and Statistics, and has taught in Austria (Fulbright Fellowship) and conducted research in Australia, Germany (junior and senior von Humbolt Foundation fellowships), Mexico and South America, and the USA. He has coauthored 5 previous books and over 200 scientific articles. Lichen Biology Second Edition Edited by THOMAS H. NASH III Arizona State University, USA CAMBRIDGE UNIVERSITY PRESS Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo Cambridge University Press The Edinburgh Building, Cambridge CB2 8RU, UK Published in the United States of America by Cambridge University Press, New York www.cambridge.org Information on this title: www.cambridge.org/9780521871624 © Cambridge University Press 1996, 2008 This publication is in copyright. Subject to statutory exception and to the provision of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press. First published in print format 2008 ISBN-13 978-0-511-41407-7 eBook (EBL) ISBN-13 978-0-521-87162-4 hardback ISBN-13 978-0-521-69216-8 paperback Cambridge University Press has no responsibility for the persistence or accuracy of urls for external or third-party internet websites referred to in this publication, and does not guarantee that any content on such websites is, or will remain, accurate or appropriate. Contents List of contri butorsvii Preface ix 1 Introduction 1 T. H. NASH III 2 Photobionts 9 T. FRIEDL AND B. BU¨ DEL 3 Mycobionts 27 R. HONEGGER 4 Thallus morphology and anatomy 40 B. BU¨ DEL AND C. SCHEIDEGGER 5 Morphogenesis 69 R. HONEGGER 6 Sexual reproduction in lichen-forming ascomycetes 94 R. HONEGGER AND S. SCHERRER 7 Biochemistry and secondary metabolites 104 J. A. ELIX AND E. STOCKER-WO¨ RGO¨ TTER 8 Stress physiology and the symbiosis 134 R. P. BECKETT,I.KRANNER, AND F. V. MINIBAYEVA 9 Physiological ecology of carbon dioxide exchange 152 T. G. A. GREEN,T.H.NASH III, AND O. L. LANGE v vi Contents 10 The carbon economy of lichens 182 K. PALMQVIST,L.DAHLMAN,A.JONSSON, AND T. H. NASH III 11 Nitrogen, its metabolism and potential contribution to ecosystems 216 T. H. NASH III 12 Nutrients, elemental accumulation, and mineral cycling 234 T. H. NASH III 13 Individuals and populations of lichens 252 D. FAHSELT 14 Environmental role of lichens 274 M. R. D. SEAWARD 15 Lichen sensitivity to air pollution 299 T. H. NASH III 16 Lichen biogeography 315 D. J. GALLOWAY 17 Systematics of lichenized fungi 336 A. TEHLER AND M. WEDIN Appendix: Culture methods for lichens and lichen symbionts 353 E. STOCKER-WO¨ RGO¨ TTER AND A. HAGER References 364 Taxon index 462 Subject index 477 Contributors Dr. Richard Beckett School of Biological and Conservation Sciences, University of Kwazulu- Natal, Private Bag X01, Pietermaritzburg, South Africa Professor Dr. Burkhard Bu¨ del Department of General Botany, Department of Biology, Erwin-Schro¨ dinger- Str. 13 University of Kaiserslautern, D-67663 Kaiserslautern, Germany Dr. Lena Dahlman Department of Ecology and Environmental Science, Umea˚University, SE- 90187 Umea˚, Sweden Emeritus Professor J. A. Elix Department of Chemistry, Faculty of Science, Australian National University, Canberra, ACT 0200, Australia Dr. Dianne Fahselt Department of Plant Sciences, University of Western Ontario, London, Ontario N6A 5B7, Canada Professor Dr. Thomas Friedl Department of Experimental Phycology and Sammlung von Algenkulturen, Albrecht-von-Haller-Institute for Plant Sciences, University of Go¨ ttingen, Untere Karspuele 2, 37073 Go¨ ttingen, Germany Dr. David Galloway 16 Farquharson St., Opoho, Dunedin, New Zealand Dr. T. G. A. Green Department of Biological Sciences, The University of Waikato, Private Bag 3105, Hamilton 3240, New Zealand Professor Dr. Rosmarie Honegger Institute of Plant Biology, University of Zu¨ rich, Zollikerstrasse 107, CH-8008 Zu¨ rich, Switzerland vii viii List of contributors Dr. Anna Jonsson Department of Ecology and Environmental Science, Umea˚University, SE-90187 Umea˚, Sweden Dr. Ilse Kranner Seed Conservation Department, Royal Botanic Gardens, Kew, Wakehurst Place, West Sussex, RH17 6TN, UK Professor Dr. Otto L. Lange Julius-von-Sachs-Institute of Biosciences, University of Wuerzburg, Lehrstuhl fuer Botanik II, Julius-von-Sachs-Platz 3, D-97082 Wuerzburg, Germany Dr. Farida Minibayeva Institute of Biochemistry and Biophysics, P.O.Box 30, Kazan, 420111, Russia Dr. Thomas H. Nash III School of Life Sciences, Arizona State University, Box 874501, Tempe, AZ 85287-4501, USA Professor Kristin Palmqvist Department of Ecology and Environmental Science, Umea˚University, SE-90187 Umea˚, Sweden Dr. Christoph Scheidegger Swiss Federal Institute for Forest, Snow and Landscape Research, WSL, Zu¨ rcherstr. 111, CH-8903 Birmensdorf, Switzerland Dr. S. Scherrer Institute of Plant Biology, University of Zu¨ rich, Zollikerstrasse 107, CH-8008 Zu¨ rich, Switzerland Professor Mark R. D. Seaward Department of Geography and Environmental Science, University of Bradford, Bradford, BD7 1DP, UK Professor Dr. Elfie Stocker-Wo¨ rgo¨ tter Department of Organismic Biology (Plant Physiology), University of Salzburg, Hellbrunner Str. 34, A-5020 Salzburg, Austria Dr. Anders Tehler Swedish Museum of Natural History, Box 50007, SE 104 05 Stockholm, Sweden Dr. Mats Wedin Swedish Museum of Natural History, Box 50007, SE 104 05 Stockholm, Sweden Preface to the second edition Twelve years ago the first edition of Lichen Biology was published, and brought a new synthesis to the field of lichenology. In the meantime, rapid advances in many areas, particularly in molecular biology, have expanded our horizons and added depth to our knowledge of areas already under investigation. Consequently, it is appropriate that a second edition has now been consummated. The original edition had 13 chapters, but this edition has 17 chapters and has added an appendix on lichen culturing, which is becoming prominent in the expanding biotechnology area. New chapters include one on sexual reproduc- tion (Chapter 6), summarizing knowledge not available in 1996. As prominent examples of stress-tolerant organisms, lichens have developed a variety of strategies that allow them to occupy both extremely cold and hot environments; consequently, these investigations were meritorious of a chapter of their own (Chapter 8). In addition, a chapter on growth (Chapter 10), a topic briefly covered in the original photosynthesis chapter, is now expanded to cover much new information and the major advances over the past decade. Although many aspects of the ecology of lichens were covered in the first edition, a number of important areas were omitted. This has been rectified in Chapter 14. Of the remaining chapters, the chapter titles remain the same from the first edition, but all chapters have been revised to a greater or lesser degree. For example, the chapter on the individual (Chapter 13) and air pollution (Chapter 15) bear little resemblance to their original counterparts. Altogether 13 additional people have contributed substantially to this edition. As with the first edition, this book should be of interest to the specialist, whether amateur or professional lichenologist. Furthermore, the book will pro- vide an essential reference for many other people, such as anyone interested in the phenomenon of symbiosis, ecologists interested in the role of lichens in ecosystems, or a land manager charged with assessing the effects of air pollution on natural systems. We also hope it will stimulate the next generation of students and young scientists to advance our knowledge of these wonderful organisms. ix 1 Introduction t. h. nash iii 1.1 The symbiosis Lichens are by definition symbiotic organisms, usually composed of a fungal partner, the mycobiont (Chapter 3), and one or more photosynthetic partners, the photobiont (Chapter 2), which is most often either a green alga or cyanobacterium. Although the dual nature of most lichens is now widely recognized, it is less commonly known that some lichens are symbioses invol- ving three (tripartite lichens) or more partners. The potential relationships of mycobionts and photobionts may in fact be quite complex (Chapter